In 1930, Copleston became a Jesuit.[1] After studying at the Jesuit novitiate in Roehampton for two years, he resettled at Heythrop, where in 1937 he was ordained a Jesuit priest at Heythrop College.[1] In 1938 he traveled to Germany to complete his training, returning to Britain just before the outbreak of war in 1939.[1] Copleston originally intended to study for his doctorate at the Gregorian University in Rome, but the war now made that impossible. Instead, he accepted an offer to return to Heythrop College to teach the history of philosophy to the few remaining Jesuits there.[1]

While teaching at Heythrop College, Copleston began writing his influential multi-volume A History of Philosophy (1946–75), a textbook that presents clear accounts of ancient, medieval, and modern philosophy.[2] Still highly respected, Copleston's history has been described as "a monumental achievement" that "stays true to the authors it discusses, being very much a work in exposition".[1]

Throughout the rest of his academic career, Copleston accepted a number of honorary roles, including Visiting Professor at Pontifical Gregorian University in Rome, where he spent six months each year lecturing from 1952 to 1968.[1] In 1970, he was made Fellow of the British Academy (FBA), and in 1972 he was given a personal professorship from Heythrop College, since re-established by the University of London. In 1975, he was made an Honorary Fellow of St. John's College, Oxford.[1]

After officially retiring in 1974, he continued to lecture. From 1974 to 1982, Copleston was Visiting Professor at the University of Santa Clara, and from 1979 to 1981, he delivered the Gifford Lectures at the University of Aberdeen, which were published as Religion and the One. These lectures were attempted to "express themes perennial in his thinking and more personal than in his history".[1] Toward the end of his life, Copleston received honorary doctorates from several institutions, including Santa Clara University, California, Uppsala University, and the University of St Andrews.[1]

In addition to his influential multi-volume History of Philosophy (1946–75), one of Copleston's most significant contributions to modern philosophy was his work on the theories of Saint Thomas Aquinas. He attempted to clarify Aquinas's Five Ways (in the Summa Theologica) by making a distinction between in fieri causes and in esse causes. By doing so, Copleston makes clear that Aquinas wanted to put forth the concept of an omnipresent God rather than a being that could have disappeared after setting the chain of cause and effect into motion.[7][8]